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Phylogeography of Habia fuscicauda (Cardinalidae) indicates population isolation, genetic divergence and demographic changes during the Quaternary climate shifts in the Mesoamerican rainforest

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Abstract

High diversity, complex topography and geological factors make the Neotropics an interesting region for the study of avian diversification. Phylogeography, in conjunction with ecological niche modeling, offers an interesting complementary approach to identify the tempo and mode of diversification in different species. In this work, we analyzed the genetic structure of Habia fuscicauda based on multilocus analyses using mtDNA (ND2 and ND4) and nuDNA (ACOI-I9 and ODC) sequences. Additionally, we transferred the optimal conditions for current distribution to the Mid-Holocene, Last Glacial Maximum and the Last Inter-Glacial in order to evaluate the shift in species distribution and compare with the genetic data. Our results indicate that H. fuscicauda comprises two clades: one with genetic correspondence to south-east Mexico to the Nicaragua Depression and the other from the south of the Nicaragua Depression to Central Panama. Within these clades, we identified genetic differentiation between populations across the Isthmus of Tehuantepec, Costa Rica—associated with the Talamanca Cordillera—and Central Panama. The two principal clades showed contrasting demographic histories, with the northern clade showing demographic changes and the southern clade demographic stasis. The ecological niche models identified areas as refugia for the northern clade fin Central America and for the southern clade in the Talamanca Cordillera and Central Panama, supporting the hypothesis that these clades were isolated from each other during the climate shifts of the Pleistocene.

Zusammenfassung

Die Phylogeographie des Rotkehlkardinals (Habia fuscicauda, Cardenalidae) zeigt Populationen-Isolierung, genetische Divergenz und demographische Veränderungen während der Klimaveränderungen im mittelamerikanischen Regenwald des Quartärs. Eine hohe Diversität, komplexe Topographie sowie geologische Faktoren machen die Neotropen zu einer interessanten Region für die Untersuchung der Artenbildung bei Vögeln. Die Phylogeographie bietet in Verbindung mit der ökologischen Nischenmodellierung einen interessanten ergänzenden Ansatz, um die Geschwindigkeit und die Art und Weise der Ausbildung verschiedener Arten zu untersuchen. In dieser Arbeit haben wir die genetische Struktur des Rotkehlkardinals (Habia fuscicauda) anhand von Multi-Locus-Sequenzanalysen unter Verwendung von mtDNA- (ND2 und ND4) und nuDNA- (ACOI-I9 und ODC) Sequenzen analysiert. Zusätzlich dazu übertrugen wir die optimalen Bedingungen für die derzeitige Verbreitung auf das Mittelholozän, das Letzteiszeitliche Maximum und die letzte Zwischeneiszeit, um die Verschiebung der Artenverteilung zu bewerten und mit den genetischen Daten zu vergleichen. Unsere Ergebnisse deuten darauf hin, dass H. fuscicauda zwei Kladen umfasst: eine mit genetischer Entsprechung im Südosten Mexikos bis zum Nicaragua-Graben und die zweite vom Süden des Nicaragua-Grabens bis nach Zentralpanama. Innerhalb dieser Kladen konnten wir genetische Unterschiede zwischen Populationen am Isthmus von Tehuantepec, in Costa Rica,—in Verbindung mit der Talamanca-Gebirgskette—und in Zentralpanama feststellen. Die beiden Hauptkladen zeigten gegensätzliche demographische Verläufe, wobei die nördliche Klade demographische Veränderungen und die südliche Klade einen demographischen Stillstand aufwies. Die ökologischen Nischenmodelle identifizierten bestimmte Gebiete als Rückzugsorte für die nördliche Klade in Mittelamerika und für die südliche Klade in der Talamanca-Gebirgskette und Zentralpanama, was die Hypothese unterstützt, dass diese Kladen während der Klimaverschiebungen im Pleistozän isoliert voneinander waren.

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Availability of data and materials

The sequences generated during the current study are available in GenBank (accession numbers: MW884324–MW884530).

Code availability

Not applicable.

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Acknowledgements

VJC-C thanks the Posgrado en Ciencias Biológicas from the Universidad Nacional Autónoma de México (UNAM) and CONACYT for the Doctoral scholarship received to perform this research, as well as the support of the scholarship “Ayudante de Investigador SNI III” (EXP. AYTE. 16804).

Funding

The research was supported by PAPIIT/DGAPA, Universidad Nacional Autónoma de México (UNAM) through a grant to Blanca E. Hernández-Baños (IN220620).

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Authors and Affiliations

  1. Departamento de Biología Evolutiva, Facultad de Ciencias, Museo de Zoología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico

    Vicente de J. Castillo-Chora & Blanca E. Hernández-Baños

  2. Posgrado en Ciencias Biológicas, Facultad de Ciencias, UNAM, Mexico City, Mexico

    Vicente de J. Castillo-Chora

  3. Museo de Zoología, Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autónoma de México, Mexico City, Mexico

    Luz E. Zamudio-Beltrán

  4. Departamento de Conservación de La Biodiversidad, El Colegio de La Frontera Sur (ECOSUR), Campeche, Mexico

    Carmen Pozo

Authors
  1. Vicente de J. Castillo-Chora
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  2. Luz E. Zamudio-Beltrán
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  3. Carmen Pozo
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  4. Blanca E. Hernández-Baños
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Contributions

BEHB and VJC-C designed the study. BEHB secured financial support. VJC-C carried out the laboratory work. BEHB, LEZB, and VJC-C analyzed the data. BEHB, VJC-C, LEZB and CP contributed to the writing and improvement of the manuscript.

Corresponding author

Correspondence to Blanca E. Hernández-Baños.

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This study was performed in line with the principles of the Declaration of Helsinki.

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Communicated by J. T. Lifjeld.

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Supplementary Information

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10336_2021_1904_MOESM1_ESM.docx

Supplementary file 1. (DOCX 69974 KB). Table SM1. GenBank accession numbers for the analyzed data and downloaded sequences used as external groups. Table SM2. Prior distribution for calibration of the main nodes used to estimate divergence times for Habia fuscicauda in Beast. Table SM3. Clean occurrence dataset for the Ecological Niche Model analysis. Table SM4. Analyses of molecular variance (AMOVA) between geographical groups NCA and LCA. Figure SM1. Model selection of bioclimatic variables and tuning of the best parameter combination for the Ecological Niche Model. a) Clustering bios in a dendrogram with 1,000 bootstrap replicates with approximately unbiased (AU) probability values (p-values). b) correlation matrix heatmap: Positive correlations are displayed in blue and negative correlations in red color. Color intensity and the size of the circle are proportional to the correlation coefficients. c) Tuning of the best parameter combination of regularization multiplier and feature types through AICc model selection. Bios: bio1 = Annual Mean Temperature; bio2 = Mean Diurnal Range; bio3 = Isothermality; bio4 = Temperature Seasonality; bio5 = Max Temperature of Warmest Month; bio6 = Min Temperature of Coldest Month; bio7 = Temperature Annual Range; bio8 = Mean Temperature of Wettest Quarter; Mean Temperature of Driest Quarter; bio10 = Mean Temperature of Warmest Quarter; bio11 = Mean Temperature of Coldest Quarter; bio12 = Annual Precipitation; bio13 = Precipitation of Wettest Month; bio14 = Precipitation of Driest Month; bio15 = Precipitation Seasonality; bio16 = Precipitation of Wettest Quarter; bio17 = Precipitation of Driest Quarter; bio18 = Precipitation of Warmest Quarter; bio19 = Precipitation of Coldest Quarter. Figure SM2. mtDNA and nDNA phylogenetic trees. Color tips indicate populations according to geographic delimitations. Polygons or symbols indicate the subspecies corresponded to each individual. Support values indicate posterior probability for Bayesian approach and bootstrap support for Maximum Likelihood. Figure SM3. Haplotype networks for the individual genes a) ND4 (mtDNA), b) ACOI-I9 (nDNA), and c) ODC (nDNA). Colors used for geographic delimitation of populations are the same as in the main text.

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Castillo-Chora, V.d., Zamudio-Beltrán, L.E., Pozo, C. et al. Phylogeography of Habia fuscicauda (Cardinalidae) indicates population isolation, genetic divergence and demographic changes during the Quaternary climate shifts in the Mesoamerican rainforest. J Ornithol 162, 961–976 (2021). https://doi.org/10.1007/s10336-021-01904-x

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